Genetic and Endocrine Contributions to Behavior and Cognition in a Working Dog Population

Abstract

The mechanisms and functions of behavior and cognition have long fascinated scientistsacross fields. This dissertation draws on recent advances in canine cognition, genetics, and endocrinology to explore the relationships between cognitive & behavioral phenotypes and genetic & hormonal variation in a working dog population. The primary phenotypic measures, from the Dog Cognitive Development Battery (DCDB), include a large number of diverse tasks designed to assess a variety of cognitive skills (e.g., human-oriented social cognition, independent problem solving, working memory, inhibitory control, perceptual discriminations), as well as temperament traits thought to be involved in social interactions and working dog success (e.g., neophobia and recovery when exposed to novel objects and startling events); we also collected behavioral survey data completed by puppy-raisers and trainers. In addition to exploring the biological bases of individual differences, this work aims to identify biological traits that contribute to working dog success and thus improve the breeding and training of working dogs, especially for assistance roles. Across three empirical chapters, this dissertation addresses unique questions aboutcognitive and behavioral associations with various biological factors using Bayesian generalized linear mixed models that control for relatedness among individuals. 1) How heritable are cognitive and behavioral phenotypes, and how do heritability estimates change over development? We find that the DCDB measures are mostly uncorrelated with each other and that phenotypes vary considerably in their heritabilities, with temperament traits being among the most heritable in both puppies (h2 = 0.32–0.61) and adults (h2 = 0.17–0.31). These heritability estimates tend to decrease over development, although whether this is solely due to age remains unclear. 2) How is structural variation in the Williams-Beuren Syndrome region associated with cognitive and behavioral phenotypes, including working dog success? This region of dog chromosome 6 was previously implicated in canine sociability and domestication in a small number of dogs and wolves. Our analyses revealed strong associations between genotypes at all four loci and certain phenotypic measures, and we found moderate differences in the genotypes of dogs who graduated versus those who did not; insertions in the gene GTF2I showed the strongest association (Beta = 0.23,CI95% = −0.04, 0.49), indicating a 1.25-fold increase in the odds of success for one insertion compared to no insertions. 3) Are basal hormone concentrations associated with individual differences in puppy behavior and cognition, and are these endocrine profiles heritable? Plasma oxytocin concentrations were associated with spatial working memory and behavioral laterality, but no credible associations were seen for social measures. Fecal cortisol concentrations were associated with decreased performance on an inhibitory control task and displayed a negative quadratic relationship with behavioral reactions to a novel object. Plasma oxytocin concentrations were very highly heritable (h2 = 0.90–0.99) and fecal cortisol concentrations were moderately-highly heritable (h2 = 0.43–0.47). This dissertation enhances our understanding of canine behavioral and cognitive phenotypes,their genetic bases, and their associations with basal hormone concentrations. This provides valuable information for the breeding and training of working dogs, although some of these results will likely be specific to this population. Furthermore, this work explores the biological mechanisms associated with behavior and cognition that might have been targets of both natural and artificial selection during domestication. Our results also add an important comparative perspective to studies in humans or laboratory model organisms. The estimated heritabilities and associations documented here lay a foundation for future studies addressing long-standing questions about the genetic and environmental contributions to dog behavior and the evolution of these traits.